Food Chemistry 258 (2018) 95–103

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Food Chemistry

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Review cattleianum fruits: A review on its composition and bioactivity T ⁎ Elisa dos Santos Pereiraa,b, Juliana Vinholesa, , Rodrigo C. Franzona, Gabriel Dalmazob, ⁎ Márcia Vizzottoa, , Leonardo Norab a Embrapa Clima Temperado, BR 392, KM 78, C. P. 403, CEP 96010-971 Pelotas, RS, Brazil b Departamento de Ciência e Tecnologia Agroindustrial, Faculdade de Agronomia Eliseu Maciel, Universidade Federal de Pelotas, Avenida Eliseu Maciel, S/N, CEP 96160–000 CapãodoLeão, RS, Brazil

ARTICLE INFO ABSTRACT

Keywords: Psidium cattleianum Sabine, commonly known as araçá, is a Brazilian native fruit, which is very juicy, with sweet Araçá to sub acid pulp and a spicy touch. The fruit can be eaten fresh or processed into juice, jellies and ice creams. Chemical composition Araçás are source of vitamin C, minerals, fatty acids, polysaccharides, volatile compounds, carotenoids and Antioxidant phenolic compounds, which can provide nutrients and phytochemical agents with different biological functions. Antidiabetic Different pharmacological studies demonstrate that P. cattleianum exerts antioxidant, antidiabetic, antic- Anticancer arcinogenic, antimicrobial, anti-inflammatory and antiaging effects. Thus, this article aims to review the che- Antimicrobial ff Anti-inflammatory mical composition and biological e ects reported for araçá fruit in the last years. Anti-aging

1. Introduction araçá-de-coroa or araçá-do-campo and in other countries are known as Cattley , Chinese guava, purple guava, yellow strawberry guava, Psidium cattleianum Sabine () is a Brazilian native species red strawberry guava, guayaba, cherry guava and lemon guava that can be found from to Rio Grande do Sul states, and also in (Bezerra, Lederman, Silva Junior, & Proença, 2010; Lisbôa, Kinupp, & the neighbor country Uruguay. It has adapted very well in tropical de Barros, 2011; Mitra, Irenaeus, Gurung, & Pathak, 2012). climates as Hawaii and many Caribbean islands (Galho et al., 2007; Flowering in south of Brazil occurs in two main times, the first from Patel, 2012). The species is characterized as a small fructiferous ever- September to October and the second in December. Eventually, a third green / (1–4 m high) whose fruit diameters are between flowering can occur in March, thus araçás can be harvest from October 2.2 cm and 5 cm, with ovoid or oblong shape, weighting less than 20 g, to March (Raseira and Raseira, 1996). Under specific conditions, araçá with high number of seeds (Biegelmeyer et al., 2011; Castro et al., orchard (0.5 m between and 4.0 m between rows of plants) can 2004). Fig. 1 shows the most common varieties of P. cattleianum fruits produce 10 ton of fruit per ha, considering 2 kg of fruit per presenting yellow and red epicarp and cream or white endocarp. (Franzon et al., 2009). However, there are also fruits with red epicarp and endocarp (Castro Araçá is very juicy fruit, with an excellent flavor and a sweet to sub et al., 2004), but they are more rare. According to the morphological acid pulp, with a spicy touch (Biegelmeyer et al., 2011). The fruit, prospection of 40 accessions of Psidium spp. (araçá) from different consumed in natura or processed (sweets, jams and juices), has high Brazilian ecoregions, 80% of fruits have cream endocarp, 11% white potential to the agri-food sector (Reissig, Vergara, Franzon, Rodrigues, and 9% pale red endocarp (Santos et al., 2010). Despite the color dif- & Chim, 2016; Santos et al., 2007). Moreover, due to the bioactivity ferences among P. cattleianum fruits varieties, they are characterized by (antiproliferative, antidiabetic and antimicrobial) of the fruit extract, a juicy core, with a translucent pulp filled with seeds. which may be related to high content of vitamin C and antioxidants, the Relevant synonyms for this species are Psidium littorale Raddi, araçá can also be valuable to the pharmaceutical industry (Franzon Eugenia ferruginea Sieber ex C. Presl, Guajava obovata (Mart. ex DC.) et al., 2009; Medina et al., 2011) Kuntze, P. ferrugineum C. Presl, P. indicum Bojer, P. obovatum Mart. ex The bioactivity reported for araçá is mainly attributed to the high DC., P. variabile O. Berg and G. cattleiana (Afzel. ex Sabine) Kuntze. content of phenolic compounds, which are well known secondary me- Nevertheless, fruits are popular known in Brazil as araçá, araçá- tabolites with high antioxidant capacity. These compounds are able to amarelo, araçá-vermelho, araçá-rosa, araçá-de-comer, araçá-da-praia, protect biological systems against the excess of free radicals and

⁎ Corresponding authors. E-mail addresses: [email protected] (J. Vinholes), [email protected] (M. Vizzotto). https://doi.org/10.1016/j.foodchem.2018.03.024 Received 17 November 2017; Received in revised form 2 March 2018; Accepted 6 March 2018 Available online 08 March 2018 0308-8146/ © 2018 Elsevier Ltd. All rights reserved. E. dos Santos Pereira et al. Food Chemistry 258 (2018) 95–103

Fig. 1. Yellow and red araçás (from: Paulo Luiz Lanzetta Aguiar). reactive oxygen species (Verma, Rajkumar, Banerjee, Biswas, & Das, essential non essential 2013). Thus, when included in human diet they contribute to reduce 80 the development of degenerative diseases such as atherosclerosis, cancer, cardiovascular diseases, diabetes among others. In addition, 60 araçá also contains other interesting chemical compounds such as mi- nerals, fatty acids, sugars, volatile compounds and carotenoids that can 40 also contribute to human health.

Prospective applications in the agri-food sector and pharmaceutical 20 industry has been reviewed by Patel (2012). Since then several studies mg/100 g of fruit have been conducted, providing knowledge to subsidize other appli- 0 cations for this species. Thus, the aim of this article was to review the literature on the biological activities and chemical composition re- Valine Serine Lysine Proline Alanine Glycine Leucine

ported for yellow and red araçá fruit in the last years. Arginine Tyrosine Cysteine Histidine Threonine Glutamine Isoleucine Methionine Asparagine Phenylalanine 2. Chemical composition Hydroxyproline Fig. 2. Essential and non-essential amino acids present in araçá. 2.1. Araçá nutritional composition Different groups of researchers studied the mineral composition of In 100 g of araçá fresh fruit there are 81.73–84.9 g of water, mature and immature yellow araçás (Table 1). Araçá from Hawaii, re- 0.75–1.03 g of protein, 0.63–1.50 g of minerals, 4.32–10.01 g of car- gardless the maturation stage, was rich in macrominerals such as po- bohydrate, 0.42–0.55 g of lipid, 3.87–6.14 g of fiber and 26.8 kcal of tassium (1.30–1.59%) and nitrogen (0.85–0.91%), and microminerals energy (Morton, 1987). When compared with apple, the most common such as iron (0.0016–0.0043%) and zinc (0.0011–0.0050%) (Adrian, fruit consumed worldwide, araçá is less caloric, lower in carbohydrate Arancon, Mathews, & Carpenter, 2015). Similar results were obtained content, and higher in lipid and dietary fiber content. for yellow and red mature araçá in Brazil (Kinupp and Inchausti, 2008; Protein content in araçá was reported to decrease in function of fruit Silva, Santos, Mendes, & Martins, 2008). Minerals are involved in me- maturation (Galho et al. 2007). Levels of protein were 93.6 mg/g and tabolic process and they have exclusive physiological function in the 39.8 mg/g dry basis, 10 and 122 days after anthesis, respectively. Fact regulation and catalyzation of important cellular mechanisms (Bailey, explained since young fruits, normally presents higher proportions of West, & Black, 2015). protoplasm in relation to dry matter Galho et al. (2007). In respect to Araçá seed contains linoleic acid as the major fatty acid in both araçá amino acids composition, there are 382 mg of total amino acids yellow and red varieties, with 61.01% ± 2.51% and and 154 mg of essential amino acids in 100 g of araçá (Hall, Smoot, 75.42% ± 3.50%, respectively. Oleic acid is present in higher amount Knight, & Nagy, 1980). Essential and non-essential amino acids present in the yellow genotype (YG) (14.99% ± 0.88%) than in red genotype in araçás are shown in Fig. 2. Leucine is the major essential amino acid (RG) (10.83% ± 0.99%). Quantitative differences for palmitic acid followed by lysine and tyrosine, isoleucine and valine while the others where observed among YG and RG, where the yellow one has are present in smaller amounts (Fig. 2)(Hall et al., 1980). Glutamine is 19.92% ± 0.26%, more than double the percentage observed in the the main non-essential amino acid followed by asparagine, alanine, red one (9.12% ± 2.12%). The content of stearic acid was low in both glycine, proline, serine, arginine and hydroxyproline (Fig. 2)(Hall genotypes, 3.57% ± 0.62% in the yellow and 4.63% ± 0.40% in the et al., 1980). The recommended intake of proteins is 0.8 g/kg/day for red one (Biegelmeyer et al., 2011). The lipid profile evaluation has an adult (19–70 years old) according to the Dietary Reference Intakes. become an important parameter since the fatty acids are crucial for the Although the araçá consumption provides a small contribution on the maintenance of a normal physiological health. Moreover, diets rich in recommended intake of proteins, it can afford relevant amounts of mono and polyunsaturated fatty acids are associated with lower risk of leucine that is the most required amino acid (42 mg/kg/day). development of cardiovascular diseases and atherosclerosis. For in- Amino acids are important compounds for the normal human body stance, linoleic acid, the most representative in araçá, exerts health function. These compounds act on cellular signaling, and are regulators benefits such as antimutagenic, anticarcinogenic (breast and skin can- of gene expression and the protein phosphorylation cascade. Besides, cers), thermogenic, antidiabetic, preventive of atherosclerosis, anti- amino acids are fundamental precursors for the syntheses of other ex- hypertensive, and stimulant of the immunological system (Koba and tremely important compounds such as hormones and low molecular Yanagita, 2014). weight nitrogenous substances (Wu, 2009).

96 E. dos Santos Pereira et al. Food Chemistry 258 (2018) 95–103

Table 1 Mineral composition of mature and immature yellow araçá and mature red araçá.

Minerals Yellow araçá Red araçá References

Mature Immature Mature

Macrominerals (%) Ca 0.14–0.21 0.15 0.18 Adrian et al. (2015), Kinupp and Inchausti (2008), Silva et al. (2008) Mg 0.11 0.12 0.08 Adrian et al. (2015), Kinupp and Inchausti (2008) N 0.85 0.91 – Adrian et al. (2015) P 0.12 0.12 0.11 Adrian et al. (2015), Kinupp and Inchausti (2008) K 1.52 1.59 1.30 Adrian et al. (2015), Kinupp and Inchausti (2008) S 0.07 0.07 0.06 Adrian et al. (2015), Kinupp and Inchausti (2008) Na 0.20 0.21 0.05 Adrian et al. (2015), Kinupp and Inchausti (2008)

Microminerals (%) B 0.0012 0.0012 0.0011 Adrian et al. (2015), Kinupp and Inchausti (2008) Cu 0.0011 0.0008 0.0006 Adrian et al. (2015), Kinupp and Inchausti (2008) Fe 0.0021–0.0039 0.0043 0.0016 Adrian et al. (2015), Kinupp and Inchausti (2008), Silva et al. (2008) Mn 0.0018 0.0011 0.0018 Adrian et al. (2015), Kinupp and Inchausti (2008) Ni 0.0001 0.0001 – Adrian et al. (2015) Zn 0.0011–0.0050 0.0011 0.0015 Adrian et al. (2015), Kinupp and Inchausti (2008)

The contents of starch, soluble carbohydrates and reducing sugars generally with a low molecular weight (< 250 Da) and high vapor were reported to increase along araçá fruit maturation. At day 122 pressure under ambient conditions, allowing them to readily diffuse (mature stage) concentrations of 89.2, 105.7 and 26.0 mg/g dry basis through the gas phase and within biological systems. In fruits, volatile were find for starch, soluble carbohydrates and reducing sugars, re- compounds are responsible for aroma characteristics, including various spectively (Galho et al., 2007). Non soluble carbohydrates, represented chemical substances (Chitarra and Chitarra, 2005). by cellulose, hemicellulose and lignin, were also evaluated by Galho The volatile composition of araçá has been reported by different et al. (2007). Contents of hemicellulose (day 10 after an- authors using different techniques such as simultaneous steam dis- thesis = 16.3 mg/g dry basis; mature stage day 122 = 9.7 mg/g dry tillation and extraction (Pino, Marbot, & Vázquez, 2001), hydro- basis) and lignin (day 10 after anthesis = 18.4 mg/g dry basis; mature distillation (Biegelmeyer et al., 2011; Marin et al., 2008) and dynamic stage day 122 = 2.8 mg/g dry basis) decreased along fruit maturation, headspace extraction (Egea, Pereira-Netto, Cacho, Ferreira, & Lopez, while cellulose do not changed (23.4 mg/g dry basis at day 10 after and 2014). 25.3 mg/g dry basis at mature stage day 122) (Galho et al., 2007). Total (E)-β-caryophyllene was the major constituent in both yellow and dietary fiber, insoluble fiber, carbohydrates, total sugar and reducing red araçá, in all studies. Nevertheless, due to the variability of the sugar contents reported by Pereira et al. (2012) for yellow genotype sample (e.g. different locations and edaphoclimatic conditions), and the was 11.95 g, 11.55 g, 15.08 g, 22.74 g and 18.6 g/100 g of dry matter, extraction method employed, the profile of yellow and red araçá is respectively. In addition, different pectin and hemicellulose compounds quite different. Apart from (E)-β-caryophyllene, hexadecanoic acid, (Z)- were found in the edible portion of the araçá fruit (mesocarp) 3-hexenol and α-pinene were the major constituents found in red araçá (Vriesmann, Lúcia, Petkowicz, & Borba, 2009). studied by (Pino et al., 2001), while β-selinene and neointermedeol The increased consumption of alimentary fibers can contribute in were those from the study of (Biegelmeyer et al., 2011). Concerning the the reduction of chronic diseases such as diabetes, cardiovascular dis- yellow araçá, neointermedeol (Marin et al., 2008), α-humulene eases and colon neoplasia (Bernaud and Rodrigues, 2013; Hur, Kim, (Biegelmeyer et al., 2011; Marin et al., 2008), β-selinene (Marin et al., Choi, & Lee, 2013; Sriamornsak, 2003). In the human diet, pectin is 2008) and geraniol (Biegelmeyer et al., 2011) were the major com- considered a dietary fiber. Different studies suggest that pectin inges- pounds. tion can reduce cholesterol and triglycerides levels, arterial tension and Although, previous work (Pino et al., 2001) did not found one or also can reduce glucose absorption. Additionally, pectin monomers, more compounds that impact the red araçá odor, they linked the araçá resulted from the microbial degradation of pectin in human intestine, flavor with the presence of aliphatic esters and terpenic compounds. was described with prebiotic effect (Nazzaro, Fratianni, Orlando, & Yellow and red araçá fruit share a common citric, green and sweet Coppola, 2012). flavor pattern, however, they were distinct according to tropical fruit characteristic, found for the YG, and tomato characteristic for the RG (Egea et al., 2014). The compound with highest impact on both yellow 2.2. Phytochemicals and red araçá odor characteristics were: (Z)-3-hexenal (grass, herbac- eous), that was the main active odorant in tomato; 1,8-cineole (minty 2.2.1. Vitamin C and eucalyptus) and (Z)-1,5-Octadien-3-one (geranium). The tropical Vitamin C, or ascorbic acid, has many physiological functions. The odor associated with the yellow araçá was supposed to be for the pre- two most important ones are its role on the increase of absorption of sence of 3-mercaptohexyl acetate with fresh and citrus aroma de- iron from vegetal origin and its high antioxidant activity, protecting the scriptors. Nevertheless, other compounds were also present and to- cell membranes and lipoproteins against the lipid peroxidation gether can explain the distinction between the two genotypes. In fact (Figueroa-Méndez and Rivas-Arancibia, 2015). Araçá is known as a rich authors attribute the odor of araçá as a result of interaction of com- source of vitamin C, with values of 200 mg and 242 mg per gram of pounds present in the fruit (Egea et al., 2014). fresh fruit, for red genotype and yellow genotype, respectively The investigation about the pharmacological activities of volatile (Luximon-Ramma, Bahorun, & Crozier, 2003). Therefore, the con- compounds has increased in the last years since different studies shows sumption of one fruit of 15 g will provide more than four times the their potential application on human health as antioxidant, hepato- recommended daily intake of vitamin C for adults. protective, anti-inflammatory, anticarcinogenic and anti-obesity, among other (Ayseli and Ayseli, 2016; Vinholes, Gonçalves, et al., 2.2.2. Volatile compounds 2014; Vinholes, Rudnitskaya, et al., 2014). (E)-β-Caryophyllene for Volatile compounds are a diverse group of organic compounds,

97 E. dos Santos Pereira et al. Food Chemistry 258 (2018) 95–103

Table 2 Carotenoids from Psidium cattleianum yellow genotype.

Compounds Concentration Reference

Yellow genotype

skin pulp whole fruit

all-trans-Antheraxanthin 9.0a 1.6a Ribeiro et al. (2014) all-trans-Lutein 10.0a 1.9a Ribeiro et al. (2014) 15.7b Silva et al. (2014) 26.4c Pereira et al. (2012)

5,6-Epoxy-β-cryptoxanthin 7.0a 2.4a Ribeiro et al. (2014) 5,8-Epoxy-β-cryptoxanthin 3.5b Silva et al. (2014) all-trans-β-Cryptoxanthin 6.0a 3.4a Ribeiro et al. (2014) 26.4 Silva et al. (2014) all-trans-α-Cryptoxanthin 3.6b Silva et al. (2014) Apocarotenoid 1.9b Silva et al. (2014) all-trans-β-Carotene 5.9a 3.7a Ribeiro et al. (2014) 20.0b Silva et al. (2014) 9-cis-β-Carotene 3.0b 1.3c Pereira et al. (2012) Silva et al. (2014) 13-cis- β-Carotene 1.2c Pereira et al. (2012) 5,6-epoxy-β-Carotene 1.2c Pereira et al. (2012) α-Carotene 4.0c Pereira et al. (2012) β-Carotene 2.9c Pereira et al. (2012) all-trans-Zeaxanthin 137.5c Pereira et al. (2012) 13′-cis-β-Cryptoxanthin phytoene 0.6b Silva et al. (2014) Cryptoxanthin 0.9c Pereira et al. (2012)

a Expressed as µg/g of extract. b Expressed as µg/100 g fresh weight. c Expressed as g/g dry matter. instance, the major volatile compound in araçá, has antioxidant (Calleja (26.4µg± 1.9µg/100gfw), all-trans-β-carotene (20.0 µg ± 4.6 µg/ et al., 2013; Elmann et al., 2009; Rather et al., 2012), anticarcinogenic, 100 g fw) and all-trans-lutein (15.7 µg ± 3.8 µg/100 g fw) (Silva, analgesic (Fidyt, Fiedorowicz, Strządała, & Szumny, 2016), hepato- Rodrigues, Mercadante, & Rosso, 2014). Although other authors found protective (Calleja et al., 2013) and neuroprotective (Chang, Kim, & similar composition, major compounds in skin and pulp were different Chun, 2007) properties. Moreover, this compound attenuates hy- being all-trans-lutein, all-trans-antheraxanthin, all-trans-β-carotene and all- perglycemia and mediated oxidative and inflammatory stress in dia- trans-β-cryptoxanthin the most representative compounds in araçá studied betic rat (Basha and Sankaranarayanan, 2016) and protects plasma and by (Ribeiro et al., 2014). Lutein was also the main carotenoid compound tissue glycoprotein components in streptozotocin-induced hypergly- in yellow araçá studied by (Pereira et al., 2012), followed by α-carotene, cemic rat (Basha and Sankaranarayanan, 2015). zeaxanthin and β-carotene. The composition of red araçá genotype is quite similar to the yellow one, as reported by Silva et al., 2014, with all-trans-β- 2.2.3. Carotenoids cryptoxanthin as a major compound, however all-trans-lutein was in the Carotenoids are a diverse group of natural pigments which have second position, and all-trans-β-carotene in the third, but with very close received considerable attention since they are potential protector values (Dalla Nora, Jablonski, et al., 2014). agents against disturbances caused by reactive oxygen species (Fiedor Carotenoids are important antioxidant compounds which ingestion and Burda, 2014). can significantly reduce the risk of diseases associated with oxidative Levels of total carotenoids in araçá vary considerably, with values of stress. The beneficial effects of carotenoids have been confirmed in 389.0–1084.0 µg and 364.4–1134.0 µg of equivalents of β-carotene/ different types of cancer, cardiovascular and eyes disorders (Fiedor and 100 g fresh weight (fw), for yellow and red araçá, respectively Burda, 2014). Improvements in baseline blood pressure, reduction of (Denardin et al., 2014; Medina et al., 2011; Vinholes, Lemos, Barbieri, inflammation and correction of dyslipidemias can also be highlighted Franzon, & Vizzotto, 2017). (Maria, Graziano, & Nicolantonio, 2015). Tables 2 and 3 presents the individual carotenoids reported in yellow and red araçá genotypes, respectively. Major individual carotenoids 2.2.4. Phenolic compounds compounds in fresh yellow araçá were all-trans-β-cryptoxanthin The total content of phenolic compounds and flavonoids, expressed in fresh weight, were reported to be more abundant in red araçá Table 3 (501.33 mg of gallic acid equivalents (GAE)/100 g and 200.20 mg of Carotenoids from Psidium cattleianum red genotype. quercetin equivalents (QE)/100 g, respectively) than in yellow one Compounds Concentrationa Reference (292.03 mg of GAE/100 g and 35.12 mg of QE/100 g, respectively) (Table 4)(Biegelmeyer et al., 2011). However, in other studies, the Red genotype total content of phenolic compounds did not differ between yellow and skin + pulp red genotypes, for instance, 5372 mg and 5638 mg of GAE acid/100 g all-trans-lutein 557.8 Dalla Nora, Jablonski, et al. (2014) and 603 mg and 606 mg of chlorogenic acid equivalent (CAE)/100 g, all-trans-β-cryptoxanthin 1029.8 were reported for YG and RG, respectively (Table 4)(Luximon-Ramma α-carotene 60.8 β et al., 2003; Vinholes et al., 2017). -carotene 512.6 ff zeaxanthin 137.5 Di erences were observed for proanthocyanidins contents (2561 mg and 2473 mg of cyanidin chloride (CE)/g in the red and in the yellow a Expressed as µg/g of extract. araçá, respectively) and flavonoids contents (712 mg of QE/g in the red

98 .dsSno eer tal. et Pereira Santos dos E.

Table 4 Total phenolic content (TPC), total flavonoid content (TFC), total proanthocyanindin content (TPAC) and total anthocyanin content (TAC) in red and yellow araçá fruits.

Study Part of the Region Year Method of extraction Red variety Yellow variety fruit TPC TFC TPAC TAC TPC TFC TPAC TAC

Biegelmeyer et al. whole Brazil – 0.75 g of grounded sample was added to 150 mL of water, heated in a water bath, 501.33a 200.20 d 292.03a 35.12d (2011) under reflux (30 min at 80 °C - 90 °C). Cooled in running water, transferred to 250 mL volumetric flask and make up to volume with water. The aqueous extract was filtered, scraping the first 50 mL of the filtrate. Luximon-Ramma et al. whole Mauritius 2000 100 g of fresh fruits, homogenized in acetone/water (70:30 v/v; 2 × 300 mL), 5638a 712e 2561f 5372 a 308e 2473f (2003) macerated (24 h, 4 °C), filtrated and residue homogenized in methanol (2 × 300 mL), macerated for 24 h, 4 °C). Acetone was removed and residue washed with dichloromethane (3 × 150 mL). Aqueous extract was concentrated in vacuum at 37 °C and reconstituted in methanol final 1:5 fresh weight/volume. 99 Vinholes et al. (2017) whole Brazil 2015 5 g of fresh fruit were homogenized with 98% ethanol (1:4, w/v) during 5 min. 606b 29.3 g 603b 1.3 g Samples were filtered and further evaporated under pressure at 40 °C. Samples were reconstituted in 20 mL of ethanol/water (3:1, v/v). Medina et al. (2011) fruit flesh Brazil – 10 g of grounded frozen pulp was extracted with 20 mL deionized water for 1 h 402.68–768.21c 4.82–6.29h 581.02–632.56c 0.21–0.55h (200 rpm) room temperature in the dark. Extracts were centrifuged (12000g, 15 min, 4 °C), the supernatant was freeze-dried and the final volume adjusted to 10 mL deionized water.

a mg of gallic acid equivalents/100 g of fresh fruit. b mg of chlorogenic acid equivalent/100 g of fresh fruit. c mg of gallic acid equivalents/100 g of fresh pulp. d mg of quercetin equivalents/100 g of fresh fruit. e mg of quercetin equivalents/g of fresh fruit. f mg of cyanidin chloride equivalents/g of fresh fruit. g mg of cyanidin-3-O-glucoside equivalents/100 g of fresh fruit. h mg of cyanidin-3-O-glucoside equivalents/100 g of fresh pulp. Food Chemistry258(2018)95–103 E. dos Santos Pereira et al. Food Chemistry 258 (2018) 95–103 araçá against 308 mg of QE/g in the yellow araçá) (Luximon-Ramma 3. Biological activities et al., 2003). The higher amount of flavonoids in the red variety can be explained by the presence of cyanidins. 3.1. Antioxidant activity The total content of phenolic compounds varies considerably be- tween different accessions. Three different accessions of red araçá In vitro studies. P. cattleianum can be considered as a good source of showed total content of phenolic compound varying from 402.68 mg to bioactive compounds with antioxidant properties (McCook-Russell, 528.30 mg of GAE/100 g fresh fruit pulp (ffp), while yellow accessions Nair, Facey, & Bowen-Forbes, 2012; Dalla Nora, Jablonski, et al., 2014). (3) varied from 581.02 mg to 632.56 mg of GAE/100 g ffp(Medina According to (Ribeiro et al., 2014), araçá is a potent scavenger of re- et al., 2011)(Table 4). Anthocyanins were present in much higher active oxygen and nitrogen species, besides its pulp has also the po- − 1 amounts in the red accessions (4.82–6.29 mg cyanidin-3-O-glucoside tential of O2 , HOCl and O2 scavenger. Similar results were obtained (C-3-O-G)/100 g ffp) than in the yellow ones (0.21–0.55 mg C-3-O-G/ by (Vinholes et al., 2017) were edible portions of araçá from yellow and − 100 g ffp) (Table 4). A similar result was observed by other author red genotypes showed good inhibition properties against O2 and hy- (Vinholes et al., 2017)(Table 4). droxyl radicals. These quantitative differences observed for total phenolic content in Fetter, Vizzotto, Corbelini, and Gonzales (2010) and Medina et al. araçá can be due to the cultivation region, edaphoclimatic conditions (2011) reported that araçá extracts with higher content of phenolic and agricultural year of the studies (Table 4). In addition, the part of the compounds where those with higher antioxidant activity. Moreover, red fruit utilized and the method of extraction can also be responsible for genotypes were more effective against DPPH than the yellow geno- the observed differences. Most of the studies used the whole fruit, with types, which authors suggest to be probably by their higher anthocya- the exception of Medina et al. (2011) who evaluated the composition of nins content. Nevertheless, results obtained in other study shows that the pulp. In respect of the method of extraction, Luximon-Ramma et al. yellow araçá (IC50 = 334.3 µg/mL ± 16.5 µg/mL) were more effective (2003) used a multi-step extraction procedure including long periods of against DPPH than the red genotype (IC50 = 490.3 µg/mL ± 35.1 µg/ maceration with solvents with different polarities and removal of fat mL) (Vinholes et al., 2017). soluble substances prior phenolic contents analysis, while other authors Araçá also showed good antioxidant protection of yeast used more simple methods (Table 4). (Saccharomyces cerevisiae) against hydrogen peroxide at a concentration Araçá studied by different groups of researchers showed a different of 25%. In fact, the action was independent of genotype and extraction individual phenolic profile (Tables 5 and 6). solvent used, and yeast survival rates were above 80% (Medina et al., The most representative phenolic compounds in yellow genotypes 2011). Hydrogen peroxide is formed during the normal cell metabolism were: gallic acid and its derivatives and ellagic acid and its derivatives and can cause damage to protein, lipid and DNA, mainly by the gen- Higher concentrations of phenolic compounds were found in the yellow eration of hydroxyl radicals through the Haber-Weiss/Fenton (Caillet araçá pulp when compared with the concentration found in the yellow et al., 2007). araçá skin (Ribeiro et al., 2014)(Table 5). Phenolic composition of red In vivo studies. Rats fed with powdered freeze-dried araçá showed araçá genotypes accounts with 9 compounds, being epicatechin and remarkable decrease on parameters altered by oxidative stress induced gallic acid the majors ones (Table 6). Although red and yellow araçá by cisplatin. Animals showed lowered levels of glucose, LDL choles- genotypes have some common phenolic compounds as described by terol, oxidized LDL cholesterol and total cholesterol when compared Medina et al. (2011), there is a lack of studies comparing the full in- with control animals (cisplatin-induced animals not feed with araçá). dividual phenolic pro file of both araçá genotypes. Also, animals fed with araçá decreased fat deposition in the liver Phenolic compounds are secondary metabolites of plants and are showing an improvement in the lipid profile (Dalla Nora, Danelli, et al., essential for their growth and reproduction. Besides, they are formed in 2014). More recently, the administration of araçá extract (200 mg/kg/ stress conditions, such as infections, wounds, UV radiations among day, for 21 days) to insulin resistant rats prevented the liver lipid per- others (Naczk and Shahidi, 2004). oxidation and the formation of reactive oxygen species (de Souza There is growing evidence that consumption of phenolic compounds Cardoso et al., 2017). present in foods may lower the risk of health disorders due to their antioxidant activity (Shahidi and Ambigaipalan, 2015). Phenolic com- 3.2. Antidiabetic activity pounds acts over reactive oxygen species and free radicals, which are in the origin of pathophysiology of neoplasia, atherosclerosis and neuro- In vitro studies. Araçá extracts were evaluated as potential inhibitor degenerative diseases (Heim, Tagliaferro, & Bobilya, 2002). In fact, of digestive enzymes and it was verified that red araçá genotypes were major phenolic compounds present in araçás (gallic acid, ellagic acid, able to inhibit alfa-glucosidase e alfa-amylase enzymes, being an al- epicatechin and quercetin), are described with chelating properties, ternative to the modulation of hyperglycemia (Pacheco, 2015). inhibition of lipid peroxidation, responsible for the maintenance of Nevertheless, araçá extracts of both genotypes were described as very endogenous antioxidant defense system, anti-inflammatory, anti- effective against alfa-glucosidase enzyme with inhibitory concentra- proliferative and antimicrobial effects among others (Badhani, Sharma, tions of 50% of the enzyme, 13 times and 16 times lower than the & Kakkar, 2015; Chanwitheesuk, Teerawutgulrag, Kilburn, & positive control (acarbose) (Vinholes et al., 2017). Rakariyatham, 2007; García-Niño and Zazueta, 2015; Jagan, In vivo studies. Administration of P. cattleianum extract (200 mg/kg/ Ramakrishnan, Anandakumar, Kamaraj, & Devaki, 2008; Kaur, day, for 21 days) prevented hyperglycemia and hypertriglyceridemia in Velmurugan, Rajamanickam, Agarwal, & Agarwal, 2009; Long et al., insulin resistant rats induced by dexamethasone (de Souza Cardoso 2016; Shay et al., 2015; Tadera, Minami, Takamatsu, & Matsuoka, et al., 2017). The mechanism of action of the extract was not reported 2006; Wang et al., 2016). Moreover, (−)-epicatechin and quercetin are by authors. Nevertheless, this activity can be related with some of the considered good inhibitors of alfa-glucosidase and alfa-amylase, key phenolic compounds present in araçá extracts, since these compounds enzymes in the control of type II diabetes mellitus (Tadera et al., 2006). are responsible for inhibiting specific enzymes (Valko et al., 2007). Procyanidins, found in both araçás genotypes, also have antidiabetic Quercetin, for instance, is considered a good inhibitor of digestive en- properties. It was found that they possess insulin mimetic functions, zymes with IC50 almost 40 times lower than the positive control reducing the hyperglycemia and stimulating the glucose absorption in (Vinholes et al., 2017). cell lines sensitive to insulin (Montagut et al., 2010). 3.3. Anticancer activity

Araçá extracts from red and yellow genotypes were tested (in vitro)

100 E. dos Santos Pereira et al. Food Chemistry 258 (2018) 95–103

Table 5 Individual phenolic compounds found in yellow araçá fruits.

Compounds Yellow References

skin pulp

Epicatechin 720.5–2659.5a Medina et al. (2011) Epicatechin epicatechin 5.4b Silva et al. (2014) Epicatechin gallate 885.0c 1603.0c Ribeiro et al. (2014) Coumaric acid 2.6–36.0a Medina et al. (2011) Ferulic acid 2.0–4.4a Medina et al. (2011) Myricetin 0.1–3.8a Medina et al. (2011) Chlorogenic acid 60.0c 121.0c Ribeiro et al. (2014) Chlorogenic acid hexoside 29.0c 26.0c Ribeiro et al. (2014) Gallic acid 464.0c 297.7–726.7a Medina et al. (2011) 1510.0c Ribeiro et al. (2014) 12.2b Silva et al. (2014) Galloyl hexoside 7.4b Silva et al. (2014) Digalloyl hexoside 2.9b Silva et al. (2014) Trigalloylquinic acid 9.0c 85.0c Ribeiro et al. (2014) Ellagic acid 2213.0c 3818.0c Ribeiro et al. (2014) Ellagic acid hexoside 136.0c 346.0c Ribeiro et al. (2014) Ellagic acid pentoside 164.0c 412.0c Ribeiro et al. (2014) Ellagic acid deoxyhexoside 1475.0c 2070.0c Ribeiro et al. (2014) Ellagitanin-like 77.0c 1022.0c Ribeiro et al. (2014) HHDP hexoside 5.7b Silva et al. (2014) Di-HHDP-hexoside 222.0c 150.0c Ribeiro et al. (2014) 4.0b Silva et al. (2014) Di-HHDP-hexoside isomer 3.9b Silva et al. (2014) HHDP digalloyl hexoside 2.3b Silva et al. (2014) HHDP digalloyl hexoside isomer 5.9b Silva et al. (2014) Quercetin 115.0c 2.0–6.8a Medina et al. (2011) 32.0c Ribeiro et al. (2014) Quercetin glucuronide 20.0c 18.0c Ribeiro et al. (2014) Quercetin hexoside 17.5c 11.4c Ribeiro et al. (2014) 6.4b Silva et al. (2014) Quercetin pentoside 39.0c 27.0c Ribeiro et al. (2014) Quercetin deoxyhexoside 53.0c 11.2c Ribeiro et al. (2014) Quercetin coumaroyl deoxyhexoside 15.0c 8.5c Ribeiro et al. (2014) Methyl ellagic acid hexoside 5.2b Silva et al. (2014) Methyl ellagic acid pentoside 5.6b Silva et al. (2014) Methyl ellagic acid deoxyhexoside 475.0c 646.0c Ribeiro et al. (2014) Methyl ellagic acid deoxyhexoside 34.0c 20.0c Ribeiro et al. (2014) Methyl ellagic acid acetyl-deoxyhexoside 10.0c 2.0c Ribeiro et al. (2014) Cinnamoyl–galloyl hexoside 573.0c 880.0c Ribeiro et al. (2014) Vanillic acid hexoside 8.1b Silva et al. (2014) Taxifolin hexoside 11.7b Silva et al. (2014) Eriodictyol hexoside 4.0b Silva et al. (2014)

a Results expressed as µg/g of fresh pulp. b Results expressed as mg/100 g of fresh pulp. c Expressed as µg/g extract.

Table 6 survival was not affected by the extracts at the highest concentration Individual phenolic compounds found in red araçá fruits. tested. This result suggests that the araçá antiproliferative effect ob- served for cancerous cells was other than toxicity. Compounds Red pulp References

– a Epicatechin 263.9 2130.4 Medina et al. (2011) 3.4. Antimicrobial activity Coumaric acid 3.3–31.7a Medina et al. (2011) Ferulic acid 3.3–8.1a Medina et al. (2011) Myricetin 0.2–14.0a Medina et al. (2011) Araçá fruit extract showed in vitro antibacterial activity against Cyanidin-3-O-glicoside 354.7b Dalla Nora, Jablonski, et al. (2014) Salmonella enteritidis, an enteric, food-borne pathogen, frequently de- b Malvidin-3-O-glicoside 243.6 Dalla Nora, Jablonski, et al. (2014) scribed in the literature on the occurrence of toxinfections in humans. Cyanidin 87.6b Dalla Nora, Jablonski, et al. (2014) – a Extracts showed minimum inhibitory concentration at 5% and it was Gallic acid 193.2 801.0 Medina et al. (2011) fi Quercetin 0.2–6.6a Medina et al. (2011) veri ed that extracts with higher secondary metabolites concentrations were more effective against the bacterial proliferation (Medina et al., a Results expressed as µg/g of fresh pulp. 2011). Intermediate activity was reported for araçá against Bacillus subtilis b Expressed as µg/g dry fruit. and Staphylococcus aureus (McCook-Russell et al., 2012). The antimicrobial activity of plants is mainly related with the presence of phenolic com- as antiproliferative agents on mammary cancer cells (MCF-7) and colon pounds in and fruits. Araçá contains flavonoids (i.e. kaempferol and cancer cells (Caco-2 cells) using rat embryonic fibroblast cells 3T3 as quercetin) and anthocyanidins (cyanidin) that are well recognized anti- control (Medina et al., 2011). Water and acetone extracts were tested at microbial agents. These compounds mode of action is related with their concentrations of 40, 60 and 80 µg/mL and it was observed a reduction reaction with microbial cellular membrane inactivating essential enzymes, on proliferation of both cancerous cells. Results were dependent of the or forming complexes with metallic ions, limiting their accessibility to the concentration and independent of genotype. In addition, control cells microbial metabolism (Medina et al., 2011).

101 E. dos Santos Pereira et al. Food Chemistry 258 (2018) 95–103

3.5. Anti-inflammatory activity Basha, R. H., & Sankaranarayanan, C. (2015). Protective role of β-caryophyllene, a ses- quiterpene lactone on plasma and tissue glycoprotein components in streptozotocin- – fl induced hyperglycemic rats. Journal of Acute Medicine, 5,9 14. http://dx.doi.org/10. The in vitro anti-in ammatory activity of araçá was tested using 1016/j.jacme.2015.02.001. hexane and ethyl acetate extracts. Reported activity at 250 μg/mL were Bernaud, F. S. R., & Rodrigues, T. C. (2013). Fibra alimentar – Ingestão adequada e efeitos 18.3% and 26.5% inhibition of ciclooxigenase-2 enzyme by hexane and sobre a saúde do metabolismo. Arquivos Brasileiros de Endocrinologia & Metabologia, 57, 397–405. http://dx.doi.org/10.1590/S0004-27302013000600001. ethyl acetate extracts, respectively (McCook-Russell et al., 2012). Au- Bezerra, J. E. F., Lederman, I. E., Silva Junior, J. F., & Proença, C. E. B. (2010). Araça. 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